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Tilapia Lake Virus: a Threat to the Global Tilapia Industry? Mona Dverdal Jansen1 , Ha Thanh Dong2 and Chadag Vishnumurthy Mohan3

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Tilapia Lake Virus: a Threat to the Global Tilapia Industry? Mona Dverdal Jansen1 , Ha Thanh Dong2 and Chadag Vishnumurthy Mohan3 Reviews in Aquaculture, 1–15 doi: 10.1111/raq.12254 Tilapia lake virus: a threat to the global tilapia industry? Mona Dverdal Jansen1 , Ha Thanh Dong2 and Chadag Vishnumurthy Mohan3 1 Norwegian Veterinary Institute, Oslo, Norway 2 Department of Microbiology, Faculty of Science, King Mongkut’s University of Technology Thonburi (KMUTT), Bangkok, Thailand 3 WorldFish, Penang, Malaysia Correspondence Abstract Mona Dverdal Jansen, Norwegian Veterinary Institute, Pb 750 Sentrum, N-0106 Oslo, Tilapia lake virus (TiLV) is a recently described virus affecting wild and farmed Norway. Email: mona-dverdal.jansen@ tilapines. At present, it has been reported on three continents (Asia, Africa and vetinst.no South America) and the number of countries where the agent has been detected is likely to increase rapidly as a result of increased awareness, surveillance and avail- Received 24 January 2018; accepted 10 April ability of diagnostic methods. Any lack of openness regarding the TiLV status of a 2018. translocating live tilapia population destined for aquaculture may inadvertently contribute to the spread of the agent. Currently, there is no cure for viral diseases in aquaculture and while vaccines and selective breeding have proved successful in reducing the severity of some viral diseases, there are currently severe knowl- edge gaps relating to TiLV and no effective, affordable vaccines are yet available. This paper summarizes the published scientific information on TiLV and high- lights important issues relating to its diagnosis, mitigation and control measures. While there have been no scientific studies on the socio-economic impact of TiLV, it may pose a significant threat particularly to small-scale fish farmers’ livelihoods and wild tilapine populations if left uncontrolled. To aid disease inves- tigations, the authors propose case definitions for suspected and confirmed cases of TiLV infections. Key words: review, syncytial hepatitis, tilapia, Tilapia lake virus. ascites and abnormal behaviour (Amal & Zamri-Saad 2011; Introduction Suwannasang et al. 2014). In 1997, it was estimated that Tilapia (Oreochromis sp.) is farmed on several continents, the yearly economic loss due to infection with Streptococ- with production ranging from extensive backyard ponds to cus was in the order of $150 million (Shoemaker & Klesius large, commercial operations. According to the Food and 1997). Apart from Streptococcosis, there are several com- Agriculture Organization of the United Nations (FAO), the mon infectious diseases in farmed tilapia. Columnaris global production of tilapia was estimated at 6.4 million caused by Flavobacterium columnare often shows clinical tons (MT) in 2015, with the top three producers being the signs of necrotic gills, fin rot, skin erosion or necrotic mus- People’s Republic of China (1.78 MT), Indonesia cle (Figueiredo et al. 2005; Dong et al. 2015a). Francisel- (1.12 MT) and Egypt (0.88 MT) (FAO 2017a). Bangladesh, losis caused by Francisella noatunensis subsp. orientalis and Vietnam and the Philippines are other leading producers Edwardsiellosis caused by Edwardsiella ictaluri produce (FAO 2017a). clinical signs of visceral white spots in internal organs (Soto Amongst the advantages of farming tilapia is its general et al. 2009, 2012; Nguyen et al. 2016). Haemorrhagic septi- hardiness, adaptability to various production systems and caemia caused by motile aeromonads (Aeromonas hy- rapid growth, with advances in genetic selection and tar- drophila, A. sobria, A. veronii and A. jandaei) may present geted breeding having further improved these characteris- clinical signs of haemorrhage, exophthalmia and ascites (Li tics (Ponzoni et al. 2011; e.g. FAO 2017b). Amongst & Cai 2011; Dong et al. 2015b, 2017d) and mixed clinical important disease challenges are Streptococcus infections, signs of complicated multiple infections (Dong et al. which affect production worldwide and can occur in most 2015b; Assis et al. 2017). A vast array of viruses have been production systems. Clinical signs of streptococcal infec- reported to affect cultured finfish (Crane & Hyatt 2011; tion may include skin haemorrhages, ocular alterations, Zhang & Gui 2015). In tilapia, several viral infections were © 2018 The Authors Reviews in Aquaculture Published by John Wiley & Sons Australia, Ltd 1 This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. M. D. Jansen et al. occasionally reported in tilapia fry including betanodavirus with TiLV as tilapia lake virus disease (OIE 2017a), other and tilapia larvae encephalitis virus (TELV) which present names such as syncytial hepatitis of tilapia (SHT) (Fergu- with neurological signs of erratic swimming or whirling son et al. 2014) and 1-month mortality syndrome (Tat- syndrome (Shlapobersky et al. 2010; Keawcharoen et al. tiyapong et al. 2017) have been used in scientific papers. 2015); infectious spleen and kidney necrosis virus (ISKNV) TiLV has been identified in samples from farms experienc- associated with gross signs of lethargy, gill pallor and dis- ing summer mortalities in Egypt (Fathi et al. 2017); how- tension of the coelomic cavity (Subramaniam et al. 2016). ever, the direct association with the virus and the summer In the late 2000s, there was a large reduction in the mortality events has not yet been determined. annual wild catch of the Israeli Sea of Galilee’s main edible In addition to scientific papers and OIE notification doc- fish, S. galilaeus, from 316 metric tons in 2005 to a low of uments, several other non-scientific documents, such as a 8 metric tons in 2009 (Eyngor et al. 2014). At the same Network of Aquaculture Centres in Asia-Pacific (NACA) time (2009), large losses of farmed tilapia were recorded disease advisory (NACA 2017) and a CGIAR Research Pro- throughout Israel (Eyngor et al. 2014). A novel RNA virus gram on Fish Agri-food Systems factsheet (CGIAR 2017), was subsequently identified and termed tilapia lake virus have been published in relation to this emerging disease (TiLV) (Eyngor et al. 2014). Subsequent to the Israeli pub- problem in an effort to notify relevant stakeholders. This lication, scientific publications have reported identification review summarizes the currently available scientific infor- of TiLV from samples collected in Colombia (Kembou Tso- mation on TiLV and highlights important research gaps fack et al. 2017), Ecuador (Ferguson et al. 2014; Bacharach and issues relating to prevention and control of the associ- et al. 2016a), Egypt (Fathi et al. 2017; Nicholson et al. ated disease. Some additional information currently only 2017), India (Behera et al. 2018), Indonesia (Koesharyani available in grey literature and through personal communi- et al. 2018), Malaysia (Amal et al. 2018) and Thailand cation has also been included for the sake of completeness. (Dong et al. 2017a; Surachetpong et al. 2017). In May 2017, the FAO released a Global Information and Early Aetiological agent Warning System (GIEWs) special alert 338 on TiLV (FAO 2017c) and the World Organization for Animal Health Viral properties (OIE) published a TiLV technical disease card (OIE 2017a). The virus has been described as a novel enveloped, nega- TiLV is currently not listed by the OIE, but there is ongoing tive-sense, single-stranded RNA virus with 10 segments work evaluating whether listing should take place. How- encoding 10 proteins (Eyngor et al. 2014; Bacharach et al. ever, TiLV is listed for reporting under the NACA regional 2016a; Surachetpong et al. 2017) and a diameter between Quarterly Aquatic Animal Diseases (QAAD) reporting 55 and 100 nm (Ferguson et al. 2014; Eyngor et al. 2014; system for the Asia-Pacific. Subsequent to the OIE publica- del-Pozo et al. 2017; Surachetpong et al. 2017; Fig. 1). All tion, six countries/territories have submitted notification 10 segments contain an open reading frame (ORF), with to the OIE of TiLV presence, namely Chinese Taipei the largest segment, segment 1, containing an open reading (OIE 2017b), Israel (OIE 2017c), Thailand (OIE 2017d), frame with weak sequence homology to the influenza C Malaysia (OIE 2017e), Peru (OIE 2018) and the Philippines virus PB1 subunit (~17% amino acid identity, 37% seg- (OIE 2017f). While the OIE terms the disease associated ment coverage) (Bacharach et al. 2016a). The remaining Figure 1 Transmission electron micrographs of TiLV-infected fish liver tissue showing cytoplasmic viral particles (white arrows) at low (a) and high (b) magnification. The electron micrograph in (b) is a magnification of the box outlined in black in (a), and the same 3 example virions (80–90 nm diameter) are indicated with white arrows in both electron micrographs (Images by H.T. Dong). Reviews in Aquaculture, 1–15 2 © 2018 The Authors Reviews in Aquaculture Published by John Wiley & Sons Australia, Ltd Tilapia lake virus threat to tilapia industry segments show no homology to other known viruses (Eyn- epithelium (del-Pozo et al. 2017). Analyses of samples orig- gor et al. 2014; Bacharach et al. 2016a); however, the con- inating from the Tanzanian and Ugandan parts of Lake served complimentary sequences at the 50 and 30 termini Victoria found TiLV RNA prevalence to be highest in the are similar to the genome organization found in orthomyx- spleen, followed by the head kidney, heart and liver oviruses (Bacharach et al. 2016a). A taxonomic
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